Functional diversity of ground beetles improved aphid control but did not increase crop yields on European farms.

Ahead of Print

Publisher: Ecological Society of America Country of Publication: United States NLM ID: 9889808 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1051-0761 (Print) Linking ISSN: 10510761 NLM ISO Abbreviation: Ecol Appl Subsets: MEDLINE

Publication: Washington, D.C. : Ecological Society of America
Original Publication: Tempe, AZ : The Society, 1991-

Land-use intensification is often associated with a decline in functional diversity, potentially undermining the provision of ecosystem services. However, how changes in traits affect ecosystem processes remains poorly understood. Variation in trait values among species in a community may drive ecosystem processes. Alternatively, the mass ratio hypothesis proposes that trait values of the dominant species in a local community are related to ecosystem processes. Using data from 159 farms in six European countries, we quantified the impact of local and landscape-level land-use intensity on ground beetles as pest control agents. We then assessed the extent to which functional diversity and community-weighted mean trait values relate to pest control and cereal yield. In addition, we assessed how the responses to land use and the effects of different species on pest control and yield varied with their traits to compare the relative impact of the traits studied. Functional diversity of ground beetles improved aphid removal, but did not translate into higher crop yields. Pest control of aphids was enhanced by a higher proportion of smaller, mobile ground beetles with a preference for the vegetation layer. Smaller, predatory ground beetles in communities improved crop yield. The magnitude of responses to land-use intensification and the effects on pest control and yield were more strongly influenced by body size than other traits. Our study provides evidence that reduced management intensity can improve pest control by supporting small-sized, macropterous ground beetles. In contrast to the claims of ecological intensification, our joint analysis of the direct effects of land use on yield and indirect effects via functional diversity of ground beetles and pest control suggests that ecosystem services by ground beetles cannot compensate for the yield gap due to a reduction in land-use intensity.
(© 2024 The Author(s). Ecological Applications published by Wiley Periodicals LLC on behalf of The Ecological Society of America.)

Arneberg, P., and J. Andersen. 2003. “The Energetic Equivalence Rule Rejected because of a Potentially Common Sampling Error: Evidence from Carabid Beetles.” Oikos 101(2): 367–375.
Bates, D., M. Maechler, B. Bolker, S. Walker, R. H. B. Christensen, H. Singmann, B. Dai, P. Green, and G. Grothendieck. 2009. “R‐Package ‘lme4’.” http://lme4.r-forge.r-project.org.
Benisch, C. 2023. “kerbtier.de – Käferfauna Deutschlands.” https://www.kerbtier.de.
Bertleff, D., J. Diekmann, S. Brand, A. G. Uenlue, and R. Bucher. 2021. “Predation and Avoidance Behaviour in Aphid‐Ladybird Interactions of Native and Invasive Ladybirds in Europe.” Ecological Entomology 46(1): 41–47.
Birkhofer, K., M. M. Gossner, T. Diekötter, C. Drees, O. Ferlian, M. Maraun, S. Scheu, et al. 2017. “Land‐Use Type and Intensity Differentially Filter Traits in Above‐ and Below‐Ground Arthropod Communities.” Journal of Animal Ecology 86: 511–520.
Birkhofer, K., C. Meub, K. Stötzel, V. Wolters, and T. Diekötter. 2015. “Optimizing Arthropod Predator Conservation in Permanent Grasslands by Considering Diversity Components beyond Species Richness.” Agriculture, Ecosystem & Environment 211: 65–72.
Birkhofer, K., H. G. Smith, W. W. Weisser, V. Wolters, and M. Gossner. 2015. “Land‐Use Effects on the Functional Distinctness of Arthropod Communities.” Ecography 38: 889–900.
Birkhofer, K., D. H. Wise, and S. Scheu. 2008. “Subsidy from the Detrital Food Web, But Not Microhabitat Complexity, Affects the Role of Generalist Predators in an Aboveground Herbivore Food Web.” Oikos 117: 494–500.
Blüthgen, N., C. F. Dormann, D. Prati, V. H. Klaus, T. Kleinebecker, N. Hölzel, F. Alt, et al. 2012. “A Quantitative Index of Land‐Use Intensity in Grasslands: Integrating Mowing, Grazing and Fertilization.” Basic and Applied Ecology 13(3): 207–220.
Bommarco, R., D. Kleijn, and S. G. Potts. 2013. “Ecological Intensification: Harnessing Ecosystem Services for Food Security.” Trends in Ecology & Evolution 28: 230–238.
Brose, U., R. B. Ehnes, B. C. Rall, O. Vucic‐Pestic, E. L. Berlow, and S. Scheu. 2008. “Foraging Theory Predicts Predator‐Prey Energy Fluxes.” Journal of Animal Ecology 77: 1072–1078.
Bucher, R., P. Batáry, J. Baudry, L. Beaumelle, A. Čerevková, E. de la Riva, T. Dirilgen, et al. 2024. “Functional Diversity of Ground Beetles Improve Aphid Control But Did Not Increase Crop Yields on European Farms.” Dryad, Dataset. https://doi.org/10.5061/dryad.pc866t1zs.
Büttner, G. 2014. “CORINE Land Cover and Land Cover Change Products.” In Land Use and Land Cover Mapping in Europe: Practices & Trends, edited by I. Manakos and M. Braun, 55–74. Dordrecht: Springer Netherlands.
Cardinale, B. J., J. E. Duffy, A. Gonzalez, D. U. Hooper, C. Perrings, P. Venail, A. Narwani, et al. 2012. “Biodiversity Loss and Its Impact on Humanity.” Nature 486: 59–67.
Carmona, C. P., I. Guerrero, M. B. Morales, J. J. Oñate, and B. Peco. 2017. “Assessing Vulnerability of Functional Diversity to Species Loss: A Case Study in Mediterranean Agricultural Systems.” Functional Ecology 31(2): 427–435.
Dainese, M., E. A. Martin, M. A. Aizen, M. Albrecht, I. Bartomeus, R. Bommarco, L. G. Carvalheiro, et al. 2019. “A Global Synthesis Reveals Biodiversity‐Mediated Benefits for Crop Production.” Science Advances 5(10): eaax0121.
de Bello, F., Z. Botta‐Dukát, J. Lepš, and P. Fibich. 2021. “Towards a more Balanced Combination of Multiple Traits When Computing Functional Differences between Species.” Methods in Ecology and Evolution 12: 443–448.
de Bello, F., S. Lavergne, C. N. Meynard, J. Lepš, and W. Thuiller. 2010. “The Partitioning of Diversity: Showing Theseus a Way Out of the Labyrinth.” Journal of Vegetation Science 21(5): 992–1000.
de la Riva, E. G., W. Ulrich, P. Batáry, J. Baudry, L. Beaumelle, R. Bucher, A. Čerevková, et al. 2023. “From Functional Diversity to Human Well‐Being: A Conceptual Framework for Agroecosystem Sustainability.” Agricultural Systems 208: 103659.
Dedryver, C. A., A. Le Ralec, and F. Fabre. 2010. “The Conflicting Relationships between Aphids and Men: A Review of Aphid Damage and Control Strategies.” Comptes Rendus Biologies 333(6–7): 539–553.
Diaz, S., and M. Cabido. 2001. “Vive la Difference: Plant Functional Diversity Matters to Ecosystem Processes.” Trends in Ecology & Evolution 16: 646–655.
Díaz, S., J. Settele, E. S. Brondízio, H. T. Ngo, J. Agard, A. Arneth, P. Balvanera, et al. 2019. “Pervasive Human‐Driven Decline of Life on Earth Points to the Need for Transformative Change.” Science 366(6471): eaax3100.
Diekötter, T., S. Wamser, V. Wolters, and K. Birkhofer. 2010. “Landscape and Management Effects on Structure and Function of Soil Arthropod Communities in Winter Wheat.” Agriculture, Ecosystem & Environment 137: 108–112.
Dray, S., and P. Legendre. 2008. “Testing the Species Traits–Environment Relationships: The Fourth‐Corner Problem Revisited.” Ecology 89(12): 3400–3412.
Emmerson, M., M. B. Morales, J. J. Oñate, P. Batáry, F. Berendse, J. Liira, T. Aavik, et al. 2016. “How Agricultural Intensification Affects Biodiversity and Ecosystem Services.” Advances in Ecological Research 55: 43–97.
Entling, M. H., K. Stämpfli, and O. Ovaskainen. 2011. “Increased Propensity for Aerial Dispersal in Disturbed Habitats Due to Intraspecific Variation and Species Turnover.” Oikos 120(7): 1099–1109.
Finke, D. L., and R. F. Denno. 2005. “Predator Diversity and Functioning of Ecosystems: The Role of Intraguild Predation in Dampening Trophic Cascades.” Ecology Letters 8: 1299–1306.
Flynn, D. F., N. Mirotchnick, M. Jain, M. I. Palmer, and S. Naeem. 2011. “Functional and Phylogenetic Diversity as Predictors of Biodiversity–Ecosystem‐Function Relationships.” Ecology 92(8): 1573–1581.
Gagic, V., I. Bartomeus, T. Jonsson, A. Taylor, C. Vinqvist, C. Fischer, E. M. Slade, et al. 2015. “Functional Identity and Diversity of Animals Predict Ecosystem Functioning Better Than Species‐Based Indices.” Proceedings of the Royal Society B 282: 20142620.
Gallé, R., and P. Batáry. 2019. “Trait‐Based Paradise—About the Importance of Real Functionality.” Community Ecology 20: 314–316.
Gallé, R., A. K. Happe, A. B. Baillod, T. Tscharntke, and P. Batáry. 2019. “Landscape Configuration, Organic Management, and Within‐Field Position Drive Functional Diversity of Spiders and Carabids.” Journal of Applied Ecology 56(1): 63–72.
Garnier, E., J. Cortez, G. Billes, M. L. Navas, C. Roumet, M. Debussche, G. Laurent, et al. 2004. “Plant Functional Markers Capture Ecosystem Properties during Secondary Succession.” Ecology 85: 2630–2637.
Garnier, E., M. L. Navas, and K. Grigulis. 2016. Plant Functional Diversity: Organism Traits, Community Structure, and Ecosystem Properties. Oxford: Oxford University Press.
Gayer, C., G. L. Lövei, T. Magura, M. Dieterich, and P. Batáry. 2019. “Carabid Functional Diversity Is Enhanced by Conventional Flowering Fields, Organic Winter Cereals and Edge Habitats.” Agriculture, Ecosystems & Environment 284: 106579.
Geiger, F., J. Bengtsson, F. Berendse, W. W. Weisser, M. Emmerson, M. B. Morales, P. Ceryngier, et al. 2010. “Persistent Negative Effects of Pesticides on Biodiversity and Biological Control Potential on European Farmland.” Basic and Applied Ecology 11(2): 97–105.
Grace, J. B., D. J. Johnson, J. S. Lefcheck, and J. E. Byrnes. 2018. “Quantifying Relative Importance: Computing Standardized Effects in Models with Binary Outcomes.” Ecosphere 9(6): e02283.
Greenop, A., B. A. Woodcock, A. Wilby, S. M. Cook, and R. F. Pywell. 2018. “Functional Diversity Positively Affects Prey Suppression by Invertebrate Predators: A Meta‐Analysis.” Ecology 99(8): 1771–1782.
Griffiths, G. J., L. Winder, J. M. Holland, C. G. Thomas, and E. Williams. 2007. “The Representation and Functional Composition of Carabid and Staphylinid Beetles in Different Field Boundary Types at a Farm‐Scale.” Biological Conservation 135(1): 145–152.
Grime, J. P., J. G. Hodgson, and R. Hunt. 1988. Comparative Plant Ecology: A Functional Approach to Common British Species. Dordrecht: Springer.
Habel, J. C., W. Ulrich, N. Biburger, S. Seibold, and T. Schmitt. 2019. “Agricultural Intensification Drives Butterfly Decline.” Insect Conservation and Diversity 12(4): 289–295.
Hanson, H., E. Palmu, K. Birkhofer, H. G. Smith, and K. Hedlund. 2016. “Agricultural Land Use Determines the Trait Composition of Ground Beetle Communities.” PLoS One 11: e0146329. https://doi.org/10.1371/journal.pone.0146329.
Hooper, D. U., F. S. I. I. I. Chapin, J. J. Ewel, A. Hector, P. Inchausti, P. Lavorel, J. H. Lawton, et al. 2005. “Effects of Biodiversity on Ecosystem Functioning: A Consensus of Current Knowledge.” Ecological Monographs 75: 3–35.
Kleijn, D., R. Bommarco, T. P. Fijen, L. A. Garibaldi, S. G. Potts, and W. H. Van Der Putten. 2019. “Ecological Intensification: Bridging the Gap between Science and Practice.” Trends in Ecology & Evolution 34(2): 154–166.
Kleijn, D., and G. I. J. Snoeijing. 1997. “Field Boundary Vegetation and the Effects of Agrochemical Drift: Botanical Change Caused by Low Levels of Herbicide and Fertilizer.” Journal of Applied Ecology 34: 1413–1425.
Kleijn, D., R. Winfree, I. Bartomeus, L. G. Carvalheiro, M. Henry, R. Isaacs, A.‐M. Klein, et al. 2015. “Delivery of Crop Pollination Services Is an Insufficient Argument for Wild Pollinator Conservation.” Nature Communications 6(1): 1–8.
Kremen, C., A. Iles, and C. Bacon. 2012. “Diversified Farming Systems: An Agroecological, Systems‐Based Alternative to Modern Industrial Agriculture.” Ecology and Society 17(4): 44.
Laliberté, E., P. Legendre, and B. Shipley. 2022. “Package ‘FD’: Measuring Functional Diversity (FD) from Multiple Traits, and Other Tools for Functional Ecology.” Version 1.0–12.1. https://cran.r-project.org/web/packages/FD/index.html.
Lavorel, S., and É. Garnier. 2002. “Predicting Changes in Community Composition and Ecosystem Functioning from Plant Traits: Revisiting the Holy Grail.” Functional Ecology 16(5): 545–556.
Lavorel, S., K. Grigulis, P. Lamarque, M. P. Colace, D. Garden, J. Girel, G. Pellet, and R. Douzet. 2011. “Using Plant Functional Traits to Understand the Landscape Distribution of Multiple Ecosystem Services.” Journal of Ecology 99: 135–147.
Lefcheck, J., J. Byrnes, and J. Grace. 2023. “piecewiseSEM: Piecewise Structural Equation Modeling.” Version 2.3.0. https://CRAN.R-project.org/package=piecewiseSEM.
Lindroth, C. H. 1985/1986. “The Carabidae (Coleoptera) of Fennoscandia and Denmark.” Fauna Entomologica Scandinavica 15: 1–225.
Lompe, A. 2023. “Käfer Europas.” https://coleonet.de/coleo/html/impressum.htm.
Loreau, M., S. Naeem, P. Inchausti, J. Bengtsson, J. P. Grime, A. Hector, D. U. Hooper, et al. 2001. “Biodiversity and Ecosystem Functioning: Current Knowledge and Future Challenges.” Science 294(5543): 804–808.
Losey, J. E., and R. F. Denno. 1998. “Positive Predator–Predator Interactions: Enhanced Predation Rates and Synergistic Suppression of Aphid Populations.” Ecology 79(6): 2143–2152.
Luka, H., W. Marggi, C. Huber, Y. Gonseth, and P. Nagel. 2009. Carabidae, Ecology – Atlas – Fauna Helvetica 24. Neuchâtel: Centre suisse de cartographie de la faune & Schweizerische Entomologische Gesellschaft. 677 pp.
Martin, E. A., M. Dainese, Y. Clough, A. Báldi, R. Bommarco, V. Gagic, M. P. Garratt, et al. 2019. “The Interplay of Landscape Composition and Configuration: New Pathways to Manage Functional Biodiversity and Agroecosystem Services across Europe.” Ecology Letters 22(7): 1083–1094.
Naeem, S., L. J. Thompson, S. P. Lawler, J. H. Lawton, and R. M. Woodfin. 1994. “Declining Biodiversity Can Affect the Functioning of Ecosystems.” Nature 368: 734–737.
Ostandie, N., L. Muneret, B. Giffard, D. Thiéry, and A. Rusch. 2021. “The Shape of the Predator Biomass Distribution Affects Biological Pest Control Services in Agricultural Landscapes.” Functional Ecology 35(1): 193–204.
Östman, Ö., B. Ekbom, and J. Bengtsson. 2001. “Landscape Heterogeneity and Farming Practice Ingluence Biological Control.” Basic and Applied Ecology 2: 365–371.
Östman, Ö., B. Ekbom, and J. Bengtsson. 2003. “Yield Increase Attributable to Aphid Predation by Ground‐Living Polyphagous Natural Enemies in Spring Barley in Sweden.” Ecological Economics 45(1): 149–158.
Pinheiro, J. 2009. “nlme: Linear and Nonlinear Mixed Effects Models.” R Package Version 3.1‐96. http://cran.r-project.org/web/packages/nlme/.
Polis, G., C. A. Myers, and R. D. Holt. 1989. “The Ecology and Evolution of Intraguild Predation: Potential Competitors that Eat Each Other.” Annual Review of Ecology and Systematics 20: 297–330.
Rader, R., I. Bartomeus, J. M. Tylianakis, and E. Laliberté. 2014. “The Winners and Losers of Land Use Intensification: Pollinator Community Disassembly Is Non‐Random and Alters Functional Diversity.” Diversity and Distributions 20(8): 908–917.
Ricotta, C., and M. Moretti. 2011. “CWM and Rao's Quadratic Diversity: A Unified Framework for Functional Ecology.” Oecologia 167: 181–188.
Roubinet, E., K. Birkhofer, G. Malsher, K. Staudacher, B. Ekbom, and M. Traugott. 2017. “Diet of Generalist Predators Reflects Effects of Cropping Season and Farming System on Extra‐ and Intraguild Prey.” Ecological Applications 27: 1167–1177.
Rusch, A., K. Birkhofer, R. Bommarco, H. G. Smith, and B. Ekbom. 2015. “Predator Body Sizes and Habitat Preferences Predict Predation Rates in an Agroecosystem.” Basic and Applied Ecology 16(3): 250–259.
Rusch, A., R. Bommarco, P. Chiverton, S. Öberg, H. Willin, S. Wiktelius, and B. Ekbom. 2013. “Response of Ground Beetle (Coleoptera, Carabidae) Communities to Changes in Agricultural Policies in Sweden over Two Decades.” Agriculture, Ecosystems & Environment 176: 63–69.
Sala, O. E., F. I. I. I. Stuart Chapin, J. J. Armesto, E. Berlow, J. Bloomfield, R. Dirzo, E. Huber Sanwald, et al. 2000. “Global Biodiversity Scenarios for the Year 2100.” Science 287(5459): 1770–1774.
Scheu, S. 2001. “Plants and Generalist Predators as Links between the Below‐Ground and Above‐Ground System.” Basic and Applied Ecology 2(1): 3–13.
Schneider, F. D., S. Scheu, and U. Brose. 2012. “Body Mass Constraints on Feeding Rates Determine the Consequences of Predator Loss.” Ecology Letters 15(5): 436–443.
Segoli, M., P. K. Abram, J. Ellers, I. C. Hardy, G. Greenbaum, G. E. Heimpel, G. E. Heimpel, et al. 2023. “Trait‐Based Approaches to Predicting Biological Control Success: Challenges and Prospects.” Trends in Ecology & Evolution 38: 802–811.
Seibold, S., M. M. Gossner, N. K. Simons, N. Blüthgen, J. Müller, D. Ambarlı, C. Ammer, et al. 2019. “Arthropod Decline in Grasslands and Forests Is Associated with Landscape‐Level Drivers.” Nature 574(7780): 671–674.
Shipley, B. 2000. “A New Inferential Test for Path Models Based on Directed Acyclic Graphs.” Structural Equation Modeling 7(2): 206–218.
Shipley, B., F. De Bello, J. H. C. Cornelissen, E. Laliberté, D. C. Laughlin, and P. B. Reich. 2016. “Reinforcing Lose Foundation Stones in Trait‐Based Plant Ecology.” Oecologia 180: 923–931.
Shipley, B., D. Vile, and E. Garnier. 2006. “From Plant Traits to Plant Communities: A Statistical Mechanistic Approach to Biodiversity.” Science 314: 812–814.
Simons, N. K., W. W. Weisser, and M. M. Gossner. 2016. “Multi‐Taxa Approach Shows Consistent Shifts in Arthropod Functional Traits along Grassland Land‐Use Intensity Gradient.” Ecology 97: 754–764.
Staudacher, K., O. Rennstam Rubbmark, K. Birkhofer, G. Malsher, D. Sint, M. Jonsson, and M. Traugott. 2018. “Habitat Heterogeneity Induces Rapid Changes in the Feeding Behaviour of Generalist Arthropod Predators.” Functional Ecology 32: 809–819.
Straub, C. S., D. L. Finke, and W. E. Snyder. 2008. “Are the Conservation of Natural Enemy Biodiversity and Biological Control Compatible Goals?” Biological Control 45: 225–237.
Tilman, D., D. Wedin, and J. Knops. 1996. “Productivity and Sustainability Influenced by Biodiversity in Grassland Ecosystems.” Nature 379: 718–720.
Török, E., S. Zieger, J. Rosenthal, R. Földesi, R. Gallé, T. Tscharntke, and P. Batáry. 2021. “Organic Farming Supports Lower Pest Infestation, but fewer Natural Enemies than Flower Strips.” Journal of Applied Ecology 58(10): 2277–2286.
Tscharntke, T., A. M. Klein, A. Kruess, I. Steffan‐Dewenter, and C. Thies. 2005. “Landscape Perspectives on Agricultural Intensification and Biodiversity – Ecosystem Service Management.” Ecology Letters 8: 857–874.
Tscharntke, T., J. M. Tylianakis, T. A. Rand, R. K. Didham, L. Fahrig, P. Batáry, J. Bengtsson, et al. 2012. “Landscape Moderation of Biodiversity Patterns and Processes‐Eight Hypotheses.” Biological Reviews 87(3): 661–685.
Turin, H. 2000. De Nederlandse Loopkevers – Verspreiding en oecologie. Leiden: Nationaal Natuurhistorisch Museum Naturalis.
Ulrich, W., P. Batáry, J. Baudry, L. Beaumelle, R. Bucher, A. Čerevková, E. G. de la Riva, et al. 2023. “From Biodiversity to Health: Quantifying the Impact of Diverse Ecosystems on Human Well‐Being.” People and Nature 5: 69–83.
Violle, C., M. L. Navas, D. Vile, E. Kazakou, C. Fortunel, I. Hummel, and E. Garnier. 2007. “Let the Concept of Trait Be Functional.” Oikos 116(5): 882–892.
Winqvist, C., J. Bengtsson, E. Öckinger, T. Aavik, F. Berendse, L. W. Clement, C. Fischer, et al. 2014. “Species' Traits Influence Ground Beetle Responses to Farm and Landscape Level Agricultural Intensification in Europe.” Journal of Insect Conservation 18: 837–846.
Wong, M. K. L., B. Guénard, and O. T. Lewis. 2019. “Trait‐Based Ecology of Terrestrial Arthropods.” Biological Reviews 94: 999–1022.
Woodcock, B. A., M. P. D. Garratt, G. D. Powney, R. F. Shaw, J. L. Osborne, J. Soroka, S. A. Lindström, et al. 2019. “Meta‐Analysis Reveals that Pollinator Functional Diversity and Abundance Enhance Crop Pollination and Yield.” Nature Communications 10(1): 1481.

2019-NC-MS-11 Environmental Protection Agency (EPA); BiodivERsA3 ERA-Net COFUND Programme (2018-2019 BiodivERsA Joint Call) (FunProd); NKFIH KKP 133839 Hungarian National Research, Development and Innovation Office; Agence Nationale de la Recherche (ANR); UMO-2019/32/Z/NZ8/00008 National Science Centre; 662944 Deutsche Forschungsgemeinschaft (DFG); FIP 16/1 Deutsche Forschungsgemeinschaft (DFG); BiodivERsA3/2018/885/FunProd Slovak Academy of Sciences

Keywords: ecological intensification; ecosystem services; landscape composition; land‐use intensity; pest control; predation; traits

Date Created: 20241007 Latest Revision: 20241007

20241007

10.1002/eap.3035

39373261